Optimizing working memory with heterogeneity of recurrent cortical excitation

Journal of Neuroscience

Volumn 33, Issue 48, 2013, Pages 18999-19011

  Kilpatrick, Zachary P ^a   Ermentrout, Bard ^b,c   Doiron, Brent ^b,c  

^a University of Houston   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CENTER FOR THE NEURAL BASIS OF COGNITION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR;

ARTICLE; BRAIN CORTEX; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE POTENTIAL; PRIORITY JOURNAL; SPIKE WAVE; SYNAPSE; SYNAPTIC POTENTIAL; WORKING MEMORY; ALGORITHM; ARTIFICIAL NEURAL NETWORK; BIOLOGICAL MODEL; CYTOLOGY; DIFFUSION; ENTROPY; HUMAN; NERVE CELL; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SHORT TERM MEMORY; STATISTICS;

ALGORITHMS; CEREBRAL CORTEX; DIFFUSION; ENTROPY; HUMANS; MEMORY, SHORT-TERM; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); NEURONS; PSYCHOMOTOR PERFORMANCE; RECEPTORS, AMPA; RECEPTORS, GABA; RECEPTORS, N-METHYL-D-ASPARTATE; STOCHASTIC PROCESSES;

EID: 84888241385     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1641-13.2013     Document Type: Article

References (64)

1. Aksay E, Major G, Goldman MS, Baker R, Seung HS, Tank DW (2003) History dependence of rate covariation between neurons during persistent activity in an oculomotor integrator. Cereb Cortex 13:1173-1184. CrossRef Medline
2. Amari S (1977) Dynamics of pattern formation in lateral-inhibition type neural fields. Biol Cybern 27:77-87. CrossRef Medline
3. Ben-Yishai R, Bar-Or RL, SompolinskyH (1995) Theory of orientation tuning in visual cortex. Proc Natl Acad Sci U S A 92:3844-3848. CrossRef Medline
4. Bogacz R, Brown E, Moehlis J, Holmes P, Cohen JD (2006) The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol Rev 113:700-765. CrossRef Medline
5. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA (1996) A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis Neurosci 13:87-100. CrossRef Medline
6. Brody CD, Romo R, Kepecs A (2003) Basic mechanisms for graded persistent activity: discrete attractors, continuous attractors, and dynamic representations. Curr Opin Neurobiol 13:204-211. CrossRef Medline
7. Brunton BW, Botvinick MM, Brody CD (2013) Rats and humans can optimally accumulate evidence for decision-making. Science 340:95-98. CrossRef Medline
8. Burak Y, Fiete IR (2012) Fundamental limits on persistent activity in networks of noisy neurons. Proc Natl Acad Sci U S A 109:17645-17650. CrossRef Medline
9. Cain N, Shea-Brown E (2012) Computational models of decision making: integration, stability, and noise. Curr Opin Neurobiol 22:1047-1053. CrossRef Medline
10. Camperi M, Wang XJ (1998) A model of visuospatial working memory in prefrontal cortex: recurrent network and cellular bistability. J Comput Neurosci 5:383-405. CrossRef Medline
11. Chelaru MI, Dragoi V (2008) Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci U S A 105:16344-16349. CrossRef Medline
12. Churchland AK, Kiani R, Chaudhuri R, Wang XJ, Pouget A, Shadlen MN (2011) Variance as a signature of neural computations during decision making. Neuron 69:818-831. CrossRef Medline
13. Clopath C, Büsing L, Vasilaki E, Gerstner W (2010) Connectivity reflects coding: a model of voltage-based stdp with homeostasis. Nat Neurosci 13:344-352. CrossRef Medline
14. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10:910-923. CrossRef Medline
15. Compte A, Constantinidis C, Tegner J, Raghavachari S, Chafee MV, Goldman-Rakic PS, Wang XJ (2003) Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task. J Neurophysiol 90:3441-3454. CrossRef Medline
16. Cover T, Thomas J (2006) Elements of information theory. New York: Wiley-Interscience.
17. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3 [Suppl]:1184-1191. Medline
18. Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9:292-303. CrossRef Medline
19. Fransén E, Tahvildari B, Egorov AV, Hasselmo ME, Alonso AA (2006) Mechanism of graded persistent cellular activity of entorhinal cortex layer V neurons. Neuron 49:735-746. CrossRef Medline
20. Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349. Medline
21. Fuster JM (1973) Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 36:61-78. Medline
22. Goldman MS, Levine JH, Major G, Tank DW, Seung HS (2003) Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron. Cereb Cortex 13:1185-1195. CrossRef Medline
23. Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14: 477-485. CrossRef Medline
24. Haefner RM, Gerwinn S, Macke JH, Bethge M (2013) Inferring decoding strategies from choice probabilities in the presence of correlated variability. Nat Neurosci 16:235-242. CrossRef Medline
25. Hansel D, Mato G (2013) Short-term plasticity explains irregular persistent activity in working memory tasks. J Neurosci 33:133-149. CrossRef Medline
26. Itskov V, Hansel D, TsodyksM (2011) Short-term facilitation may stabilize parametric working memory trace. Front Comput Neurosci 5:40. CrossRef Medline
27. Kilpatrick ZP, Ermentrout B (2013) Wandering bumps in stochastic neural fields. SIAM J Appl Dyn Syst 12:61-94. CrossRef
28. Klingberg T (2010) Training and plasticity of working memory. Trends Cogn Sci 14:317-324. CrossRef Medline
29. Ko H, Hofer SB, Pichler B, Buchanan KA, Sjöström PJ, Mrsic-Flogel TD (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473:87-91. CrossRef Medline
30. Ko H, Cossell L, Baragli C, Antolik J, Clopath C, Hofer SB, Mrsic-Flogel TD (2013) The emergence of functional microcircuits in visual cortex. Nature 496:96-100. CrossRef Medline
31. Koulakov AA, Raghavachari S, Kepecs A, Lisman JE (2002) Model for a robust neural integrator. Nat Neurosci 5:775-782. CrossRef Medline
32. Laing C, Lord GJ (2009) Stochastic methods in neuroscience. New York: Oxford UP.
33. Laing CR, Chow CC (2001) Stationary bumps in networks of spiking neurons. Neural Comput 13:1473-1494. CrossRef Medline
34. Lewis DA, Gonzalez-Burgos G (2000) Intrinsic excitatory connections in the prefrontal cortex and the pathophysiology of schizophrenia. Brain Res Bull 52:309-317. CrossRef Medline
35. Lifson S, Jackson JL (1962) On self-diffusion of ions in a polyelectrolyte solution. J Chem Phys 36:2410.
36. Lindner B, Kostur M, Schimansky-Geier L (2001) Optimal diffusive transport in a tilted periodic potential. Fluct Noise Lett 1:R25-R39. CrossRef
37. Luck SJ, Vogel EK (1997) The capacity of visual working memory for features and conjunctions. Nature 390:279-281. CrossRef Medline
38. Marsat G, Maler L (2010) Neural heterogeneity and efficient population codes for communication signals. J Neurophysiol 104:2543-2555. CrossRef Medline
39. McNab F, Varrone A, Farde L, Jucaite A, Bystritsky P, Forssberg H, Klingberg T (2009) Changes in cortical dopamine d1 receptor binding associated with cognitive training. Science 323:800-802. CrossRef Medline
40. Meyer T, Qi XL, Stanford TR, Constantinidis C (2011) Stimulus selectivity in dorsal and ventral prefrontal cortex after training in working memory tasks. J Neurosci 31:6266-6276. CrossRef Medline
41. Miller P (2006) Analysis of spike statistics in neuronal systems with continuous attractors or multiple, discrete attractor states. Neural Comput 18: 1268-1317. CrossRef Medline
42. Osborne LC, Palmer SE, Lisberger SG, BialekW (2008) The neural basis for combinatorial coding in a cortical population response. J Neurosci 28: 13522-13531. CrossRef Medline
43. Padmanabhan K, Urban NN (2010) Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 13:1276-1282. CrossRef Medline
44. Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA (2002) Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 5:805-811. CrossRef Medline
45. Ploner CJ, Gaymard B, Rivaud S, Agid Y, Pierrot-Deseilligny C (1998) Temporal limits of spatial working memory in humans. Eur J Neurosci 10: 794-797. CrossRef Medline
46. Polk A, Litwin-Kumar A, Doiron B (2012) Correlated neural variability in persistent state networks. Proc Natl Acad Sci U S A 109:6295-6300. CrossRef Medline
47. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81:1903-1916. Medline
48. Renart A, Song P, Wang XJ (2003) Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron 38:473-485. CrossRef Medline
49. Ringach DL, Shapley RM, Hawken MJ (2002) Orientation selectivity in macaque V1: diversity and laminar dependence. J Neurosci 22:5639-5651. Medline
50. Risken H (1996) The Fokker-Planck equation: methods of solution and applications, volume 18. Berlin: Springer.
51. Romo R, Brody CD, Hernández A, Lemus L (1999) Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399:470-473. CrossRef Medline
52. Rosen MJ (1972) A theoretical neural integrator. IEEE Trans Biomed Eng 19:362-367. Medline
53. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27. Medline
54. Shamir M, Sompolinsky H (2006) Implications of neuronal diversity on population coding. Neural Comput 18:1951-1986. CrossRef Medline
55. Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6:389-397. CrossRef Medline
56. Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19:9587-9603. Medline
57. Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24:455-463. CrossRef Medline
58. Wang XJ (2008) Decision making in recurrent neuronal circuits. Neuron 60:215-234. CrossRef Medline
59. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, Goldman-Rakic PS (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 9:534-542. CrossRef Medline
60. Wei Z, Wang XJ, Wang DH (2012) From distributed resources to limited slots in multiple-item working memory: a spiking network model with normalization. J Neurosci 32:11228-11240. CrossRef Medline
61. White JM, Sparks DL, Stanford TR (1994) Saccades to remembered target locations: an analysis of systematic and variable errors. Vision Res 34:79-92. CrossRef Medline
62. Wilken P, Ma WJ (2004) A detection theory account of change detection. J Vis 4(12):1120-1135. Medline
63. Wu S, Hamaguchi K, Amari S (2008) Dynamics and computation of continuous attractors. Neural Comput 20:994-1025. CrossRef Medline
64. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112-2126. Medline